Influence of ocean and freshwater conditions on Columbia River sockeye salmon Oncorhynchus nerka adult return rates

In recent years, returns of adult sockeye salmon Oncorhynchus nerka to the Columbia River Basin have reached numbers not observed since the 1950s. To understand factors related to these increased returns, we first looked for changes in freshwater production and survival of juvenile migrants. We then evaluated productivity changes by estimating smolt‐to‐adult return rates (SAR) for juvenile migration years 1985–2010. We found SAR varied between 0.2 and 23.5%, with the highest values coinciding with recent large adult returns. However, the largest adult return, in 2012, resulted not from increased survival, but from increased smolt production. We evaluated 19 different variables that could influence SARs, representing different facets of freshwater and ocean conditions. We used model selection criteria based on small‐sample corrected AIC to evaluate the relative performance of all two‐ and three‐variable models. The model with April upwelling, Pacific Northwest Index (PNI) in the migration year, and PNI in the year before migration had 10 times the AIC_c weight as the second‐best‐supported model, and R² = 0.82. The variables of April ocean upwelling and PNI in the migration year had high weights of 0.996 and 0.927, respectively, indicating they were by far the best of the candidate variables to explain variations in SAR. While our analyses were primarily correlative and limited by the type and amount of data currently available, changes in ocean conditions in the northern California Current system, as captured by April upwelling and PNI, appeared to play a large role in the variability of SAR.     

Simulation of juvenile sockeye salmon (Oncorhynchus nerka) migrations in the Strait of Georgia, British Columbia

Previous research has documented two main migratory routes of juvenile sockeye salmon (Oncorhynchus nerka) through the Strait of Georgia, British Columbia, Canada, and large interannual variability in marine survival rates of the Chilko Lake stock. Simulation models were used to explore the influence of surface currents on the migratory route of juvenile sockeye salmon (smolts) through the Strait of Georgia. We used a model of downstream migration to generate daily numbers of Chilko Lake sockeye salmon smolts entering the Strait of Georgia, based on daily counts of smolts leaving the rearing lake. A numerical hydrodynamic model (driven by surface wind, tide, and Fraser River discharge) hindcasted surface currents in the Strait of Georgia on a 2 km × 2 km grid. A smolt migration model simulated fish moving through the Strait with different compass-oriented migratory behaviours (i.e. swimming speed and directional orientation) within the time-varying surface advection field. Results showed that surface currents within the Strait of Georgia can affect the migratory route of sockeye salmon smolts in spite of their large size (8 cm). Wind is the forcing mechanism primarily responsible for determining which migratory route would be used. Under prevailing wind conditions (i.e. toward the north-west), most sockeye salmon smolts would use the eastern migratory route; however, relatively brief south-eastward wind events (lasting about 2 days) would force most smolts into the western migratory route. Given the heterogeneity of food for salmon within the Strait, we hypothesize that wind-driven variability in the annual proportion of smolts that use the western and eastern migratory routes in the Strait of Georgia affects early marine survival rates of Fraser River sockeye salmon.     

A matter of timing: the role of ocean conditions in the initiation of spawning migration by late‐run Fraser River sockeye salmon (Oncorhynchus nerka)

Year 1995 marked the start of a major shift to earlier river entry of late‐run Fraser River sockeye salmon (Oncorhynchus nerka) en route to the spawning grounds. Earlier entry has typically been accompanied by considerably greater in‐river mortality. We examine this behavioral change using correlation analyses between the entry timing of the Adams River and Weaver Creek stocks and the surface marine conditions encountered by the stocks during their homing migration from the northeast Pacific several months earlier. For Adams stocks, maximum correlation is between entry timing and offshore winds, such that the weaker the wind stress in the direction of the prevailing surface currents in early July, the earlier the river entry in late summer. For Weaver stocks, maximum correlation is with salinity, such that the lower the surface salinity along the coast in August, the earlier the river entry. We hypothesize that oceanic changes lead to changes in late‐run sockeye physiology which then leads to changes in behavior. Physiological changes are postulated to arise from two types of preconditioning: Type‐1 occurs in the offshore region, whereby the weaker the prevailing currents that normally hinder eastward migration, the more endogenous energy available for maturation and the earlier the river entry. Type‐2 occurs in coastal regions, whereby the lower the salinity, the more rapid the osmoregulatory adaptation to freshwater (and possible susceptibility to water‐borne pathogens) and the earlier the entry. Results suggest that the earlier entry that began in the mid‐1990s is linked to weaker ocean currents and lower coastal salinities.     

Influence of the marine abundance of pink (Oncorhynchus gorbuscha) and sockeye salmon (O. nerka) on growth of Ozernaya River sockeye

The length and weight of Russian sockeye ( Oncorhynchus nerka ) returning to the Ozernaya River (Kamchatka) was substantially reduced in years when the ocean abundances of Kamchatkan pink ( O. gorbuscha ) and sockeye salmon were high. We found that the density-dependent reduction in sockeye growth on a per-capita basis was greater for sockeye than for pink salmon. However, the overall effect of pink salmon abundance on sockeye growth was greater because of the higher numerical abundance of pink salmon. The strongest statistical relationships were found for sockeye from separate age groups; pooled data combining all age classes were statistically insignificant. We estimate that, if pink salmon were absent, the most strongly affected age group of sockeye salmon (2.1 males) would weigh twice as much at maturity than if pink salmon populations from eastern and western Kamchatka were both simultaneously at peak observed abundances. Trophic competition in the ocean between pink and sockeye salmon can therefore have a significant influence on the productivity of sockeye populations for the most strongly affected age groups. These effects are large enough that they should be explicitly considered in the management of salmon populations.     

Somatic energy of sockeye salmon Oncorhynchus nerka at the onset of upriver migration: a comparison among ocean climate regimes

We examined somatic energy patterns in two stocks (Chilko and Early Stuart) of adult Fraser River (British Columbia, Canada) sockeye salmon (Oncorhynchus nerka), collected at the end of their ocean residency, spanning years across different climate regimes. Both stocks had high levels of somatic energy in years with high open ocean productivity (1956, 1957, 2001 and 2002), and relatively low levels in years with poor open ocean productivity (1999 and 2000). For Early Stuart sockeye, energy levels in 1999 and 2000 were approximately 15% lower (～1.5 MJ kg^?1) than that in the 1950s, an amount of energy equivalent to that necessary for migrating 600 km upriver. In recent years (2001 and 2002), energy levels have increased by about 9% for both stocks. Low energy levels at the onset of upriver migration, particularly in years of energetically demanding in‐river conditions, such as high flows or temperatures, are likely to contribute to prespawning and en route mortality in Fraser sockeye.     

Challenges for the Kasatoshi volcano hypothesis as the cause of a large return of sockeye salmon (Oncorhynchus nerka) to the Fraser River in 2010

In August 2008 the Kasatoshi volcano in the Aleutian archipelago erupted. Prevailing winds carried volcanic ash to the Gulf of Alaska, where its soluble iron dissolved and initiated a widespread phytoplankton bloom. Two years later, the abundance of sockeye salmon (Oncorhynchus nerka) returning to spawn in the Fraser River was larger than any observed since 1913. Kasatoshi's influence on growth and survival has been proposed as the ultimate cause of the abundant return. However, when relevant data are brought to bear on the hypothesis, it shows that: (1) survival of the abundant sockeye salmon cohort was unremarkable when compared with the historical record; (2) without an accompanying volcano, survival of the returns in 2011 was about the same as in 2010; (3) parental abundance that spawned the abundant return in 2010 was the sixth largest since 1948; (4) during their first summer at sea, sockeye salmon are not known to migrate in the offshore region where the anomalous chlorophyll bloom occurred; (5) an older cohort that was likely exposed to the chlorophyll bloom had the second lowest productivity on record when it returned in 2009; (6) immature sockeye salmon do not feed on diatoms, so any trophodynamic benefit derived from excess chlorophyll in mid‐to late August 2008 would have to have found a rapid trophic pathway to sockeye salmon on the continental shelf; and (7) no other populations of sockeye salmon or other species of salmon that are known to rear in the same region had unexpectedly high returns.     

An investigation of the biological basis of return variability for sockeye salmon (Oncorhynchus nerka) from Great Central and Sproat lakes,Vancouver Island

We tested whether variations in stock characteristics (spawner and smolt abundance) and biotic conditions (prey variability, predation, competition) during the early marine period explained variations in the return of sockeye salmon (Oncorhynchus nerka) to Great Central and Sproat lakes, adjacent lakes on the west coast of Vancouver Island. There are two freshwater age groups in each lake; fish spend 1 or 2 yrs in freshwater after hatching. We tested the influences of stock and biotic factors on the return of each of the two age groups from each of the two lakes. Results of regression analyses showed that prey biomass variability best explained the variation in return for all lake‐age groups. Euphausiid (Thysanoessa spinifera) and cladoceran (Evadne) prey biomass variability explained between 0.75 and 0.95 (adjusted R²) of the variation in return. There appear to be instances of a mismatch between the seasonality of prey productivity and the apparent critical period of feeding for juvenile sockeye.     

On the effect of the Kasatoshi volcano on the large return of sockeye salmon (Oncorhynchus nerka) to the Fraser River in 2010

The hypothesis on the beneficial effect of volcanic ash on sockeye salmon (Oncorhyncus nerka) survival, advanced in an earlier paper (Parsons and Whitney, 2012), is discussed further in the light of a response on this subject by McKinnell (Fish. Oceanogr., 22, 2013, 337–344). We elaborate on a number of points which challenge our original hypothesis.     

Long-term changes in rearing habitat and downstream movement by juvenile sockeye salmon (Oncorhynchus nerka) in an interconnected Alaska lake system

Abstract –  In some populations the phenomenon of partial migration develops where some individuals stay in a given habitat rather than move with the migratory component. Depending on the selective pressures, the individuals that stay may be larger, smaller or similar in size to those that move. Freshwater movements of juvenile sockeye salmon ( Oncorhynchus nerka Walbaum) fry vary among and within populations, and can be complex, especially in interconnected lake systems. We examined variation of movement patterns by a sockeye salmon population in an interconnected lake system during a period of rapid natural habitat change and found that fry migrating downstream were shorter, had lower body condition, and were more likely ill and moribund compared with fish remaining in the lake. However, otolith microstructure measurements indicated that emigrants did not grow significantly slower than residents prior to downstream movement. We show that patterns (i.e., demography of migrants, timing of movement) of downstream movement have changed since the 1970s, corresponding to changes in rearing habitat. Our findings parallel the results with other salmonid species and are generally consistent with the paradigm that density-dependent interactions from declining habitat availability or quality result in the downstream movement of competitively inferior individuals, although the mechanisms governing downstream migration are unclear in this system.     

Synergistic osmoregulatory dysfunction during salmon lice (Lepeophtheirus salmonis) and infectious hematopoietic necrosis virus co‐infection in sockeye salmon (Oncorhynchus nerka) smolts

While co‐infections are common in both wild and cultured fish, knowledge of the interactive effects of multiple pathogens on host physiology, gene expression and immune response is limited. To evaluate the impact of co‐infection on host survival, physiology and gene expression, sockeye salmon Oncorhynchus nerka smolts were infected with the salmon louse Lepeophtheirus salmonis (V?/SL+), infectious hematopoietic necrosis virus (IHNV; V+/SL?), both (V+/SL+), or neither (V?/SL?). Survival in the V+/SL+ group was significantly lower than the V?/SL? and V?/SL+ groups (p = 0.024). Co‐infected salmon had elevated osmoregulatory indicators and lowered haematocrit values as compared to the uninfected control. Expression of 12 genes associated with the host immune response was analysed in anterior kidney and skin. The only evidence of L. salmonis‐induced modulation of the host antiviral response was down‐regulation of mhc I although the possibility of modulation cannot be ruled out for mx‐1 and rsad2. Co‐infection did not influence the expression of genes associated with the host response to L. salmonis. Therefore, we conclude that the reduced survival in co‐infected sockeye salmon resulted from the osmoregulatory consequences of the sea lice infections which were amplified due to infection with IHNV.     

Site fidelity of spawning sockeye salmon (Oncorhynchus nerka W.) in the presence and absence of olfactory cues

Abstract –  We examined the site fidelity of spawning adult sockeye salmon ( Oncorhynchus nerka ) by tagging and releasing fish in the same stream reach (controls) and displacing them among different but nearby sites ( c . 50 m away). Three sites – two above a stream junction ('upper' reach and 'pond') and one below ('lower' reach) – allowed us to compare the behavior of salmon in the presence and absence of olfactory cues and habitat similarity. Most controls of both sexes (90%) remained in the immediate vicinity of the tagging and release site. When displaced downstream, where the odors of both the upper reach and the pond were detectable, most salmon returned to their former site (65%). Displaced sockeye were more likely to return to the pond from the lower reach than from the upper one ( P  = 0.05), consistent with olfactory orientation and the hypothesis that salmon prefer certain habitats. Salmon displaced from the upper to the lower reach were much more likely to return than those displaced to the pond ( P  < 0.01), consistent with the role of odors in orientation and inconsistent with the habitat choice hypothesis.     

Competition between Asian pink salmon (Oncorhynchus gorbuscha) and Alaskan sockeye salmon (O. nerka) in the North Pacific Ocean

The importance of interspecific competition as a mechanism regulating population abundance in offshore marine communities is largely unknown. We evaluated offshore competition between Asian pink salmon and Bristol Bay (Alaska) sockeye salmon, which intermingle in the North Pacific Ocean and Bering Sea, using the unique biennial abundance cycle of Asian pink salmon from 1955 to 2000. Sockeye salmon growth during the second and third growing seasons at sea, as determined by scale measurements, declined significantly in odd‐numbered years, corresponding to years when Asian pink salmon are most abundant. Bristol Bay sockeye salmon do not interact with Asian pink salmon during their first summer and fall seasons and no difference in first year scale growth was detected. The interaction with odd‐year pink salmon led to significantly smaller size at age of adult sockeye salmon, especially among younger female salmon. Examination of sockeye salmon smolt to adult survival rates during 1977–97 indicated that smolts entering the ocean during even‐numbered years and interacting with abundant odd‐year pink salmon during the following year experienced 26% (age‐2 smolt) to 45% (age‐1 smolt) lower survival compared with smolts migrating during odd‐numbered years. Adult sockeye salmon returning to Bristol Bay from even‐year smolt migrations were 22% less abundant (reduced by 5.9 million fish per year) compared with returns from odd‐year migrations. The greatest reduction in adult returns occurred among adults spending 2 compared with 3 years at sea. Our new evidence for interspecific competition highlights the need for multispecies, international management of salmon production, including salmon released from hatcheries into the ocean.     

Effects of Rhizopus extract administration on somatic growth and sexual maturation in lacustrine sockeye salmon Oncorhynchus nerka

ABSTRACT: The filamentous fungi Rhizopus , like many fungal species, possesses physiologically active substances. Rhizopus extract (RU) is reported to be effective for various aspects of growth and reproduction in many vertebrates. The effects of RU administration on body growth and plasma levels of steroid hormones were investigated in lacustrine sockeye salmon Oncorhynchus nerka . One-year-old fish were fed daily with RU (20 mg/kg feed) from July 1999 to October 2000 for 15 months. Fish were sampled every month and plasma levels of testosterone (T), 11-ketotestosterone (11-KT), estradiol-17β (E₂) and 17α,20β-dihydroxy-4-pregnen-3-one (DHP) were measured by time-resolved fluoroimmunoassay. Body growth of RU-fed fish of both sexes increased significantly in 1⁺ and 2⁺ October, and 2⁺ January–March and July. All RU-fed males and one female matured in 2⁺ October. RU-fed 1⁺ precociously mature males showed increased plasma levels of T, 11-KT and DHP in 1⁺ October. In 2⁺ males, RU significantly elevated plasma levels of T from May to June, 11-KT from June to July, and DHP in October. In sockeye salmon, administration of RU accelerated body growth of both sexes and sexual maturation in males, suggesting physiologically active substances present in RU enhance somatic growth and sexual maturation by sex-specific mechanisms.     

Assessing the northern diversion of sockeye salmon returning to the Fraser River, BC

We examine the oft-quoted relationship between the migration of Fraser River sockeye salmon around the northern end of Vancouver Island and sea surface temperatures. We examine the methods used to estimate the northern diversion and conclude that the estimates have a sufficiently low expected error to form a useful representation of sockeye salmon behaviour. The well-known relationship with Kains Island sea surface temperature is explored and problems are pointed out. In particular, we explore why Kains Island temperatures are good predictors of salmon behaviour in May when the sockeye can be over 1000 km away, but the coastal temperatures are poor predictors in July to September when the salmon are actually close by. We show that a more robust predictor can be developed using open ocean temperature fields and we show why Kains Island fails as a predictor during the summer months. Finally, we show by cross-validation that the northern diversion is predictable with an r.m.s. error of about 0.1.     

The relationships between fish health, metabolic rate, swimming performance and recovery in return-run sockeye salmon, Oncorhynchus nerka (Walbaum)

The repeat swimming ability and oxygen uptake (Mo2) of adult sockeye salmon, Oncorhynchus nerka (Walbaum), were assessed at ambient water temperatures at three field locations along their migration route. Following these measurements, internal and external fish condition was evaluated according to United States Environmental Protection Agency guidelines. Here we report on the physiological characteristics of fish having either moderate or severe levels of disease and injury. Routine oxygen uptake (Mo2) did not differ between healthy fish and those with indices of ill health. In contrast, fish classified as sick, which included conditions of damaged internal organs, an Ichthyophonus spp. heart infection, a Saprolegnia spp. gill infection, and skin wounds, had a lower post-exercise Mo2 and were unable to repeat their critical swim speed (U(crit)) on the second swim test. Moderate levels of disease or injury did not significantly affect either U(crit) or post-exercise Mo2. We conclude that the ability of adult salmon to recover quickly from exercise may be a useful indicator of sublethal pathologies.     

Temperature-mediated en route migration mortality and travel rates of endangered Snake River sockeye salmon

Abstract  Conservation efforts for endangered Snake River sockeye salmon ( Oncorhynchus nerka ) have been hindered by high en route adult mortality during their ∼1450 km freshwater spawning migration. Identifying causal factors for this mortality has been difficult given very small (often <10 fish) annual returns in recent decades. However, several hundred hatchery-bred fish returned in 2000 and we intercepted and radio-tagged 31 in mid-migration to monitor behaviours and survival. All fish initially migrated at similar rates, but later-timed fish eventually slowed migration and were far more likely to be unsuccessful. Late-season mortality was strongly associated with water temperatures near tolerance thresholds (21–24 °C). The data also suggest increased risk for fish in poor initial condition (i.e., with injuries or parasites) and probable recent selection against late-timed salmon. Results parallel temperature- and condition-related adult mortality in Columbia and Fraser River sockeye salmon populations and demonstrate the potential vulnerability of marginal southern populations to regional climate warming.     

Seasonal changes of hormones and muscle enzymes in adult lacustrine masu (Oncorhynchus masou) and sockeye salmon (O. nerka)

The upstream migration of adult anadromous fishes is characterized by physiological changes in responses to reproductive and energetic challenges. This study analyzed the physiological responses of lake-resident anadromous masu salmon (Oncorhynchus masou) and sockeye salmon (O. nerka) to migration in order to determine if these fish might serve as a suitable model for ocean-running populations and to differentiate between physiological responses to reproduction and to exercise-linked aspects of migration. Reproductive (estradiol, testosterone, 11-ketotestosterone, 17α,20β-dihydroxy-4-pregnen-3-one) and metabolically-linked (thyroxine, triiodothyronine) hormones showed similar patterns to ocean-running anadromous populations. White muscle pyruvate kinase, lactate dehydrogenase and malate dehydrogenase decreased with the onset of spawning season while white muscle citrate synthase, β-hydroxyacetyl CoA dehydrogenase, phosphofructokinase and glutamate oxaloacetate transaminase did not, suggesting that the former group of enzymes are responding to reproductive or food intake signals while the second group, which typically change during anadromous migration, may be responding to exercise-linked aspects of migration. This revised version was published online in August 2006 with corrections to the Cover Date.     

An evaluation of the potential influence of SST and currents on the oceanic migration of juvenile and immature chum salmon (Oncorhynchus keta) by a simulation model

Using a salmon migration model based on the assumption that swimming orientation is temperature dependent, we investigated the determining factors of the migration of juvenile and immature chum salmon (Oncorhynchus keta) in the North Pacific. We compared the predictions of the model with catch data of immature and juvenile chum salmon collected by Japanese research vessels from 1972 to 1999. The salmon migration model reproduced the observed distributions of immature chum salmon and indicates that passive transport by wind‐driven and geostrophic currents plays an important role in the eastward migration of Asian salmon. These factors result in a non‐symmetric distribution of Asian and North American chum salmon in the open ocean. The directional swimming component contributes to the northward migration in summer. The model results indicate that during the first winter Asian chum salmon swim northward against the southward wind‐driven currents to stay in the western North Pacific. This suggests that Asian chum salmon require more energy to migrate than other stocks during the first winter of their ocean life.     

Changes in plasma somatolactin levels during spawning migration of chum salmon (Oncorhynchus keta)

Plasma somatolactin (SL) concentrations were examined in chum salmon in relation to gonadal maturation; immature salmon in the Bering Sea at various stages of maturation, and mature salmon during upstream migration caught at the ocean, bay and river. Plasma SL concentrations as well as plasma prolactin (PRL) and growth hormone (GH) levels in the immature fish caught in the Bering Sea were maintained essentially at similar levels. Plasma SL in mature salmon increased significantly from the fish in the ocean to the fish in the river in both sexes. Although all the fish had fully developed gonads, females completed ovulation while still in the bay, whereas final spermeation in males was achieved after entry into the river. Thus, no clear correlation was seen between plasma SL levels and final gonadal maturation. On the other hand, plasma PRL concentrations in both male and female fish were higher in the fish in the river than those in the ocean and bay, and plasma GH levels were higher in both sexes in the fish in the bay and river than those in the ocean. Plasma levels of triglycerides, glucose, free fatty acids and ionized sodium and calcium were also examined. Significant-negative correlations were seen between plasma SL and plasma ionized calcium in mature male salmon, and between plasma SL and plasma triglycerides in mature female salmon. Although our findings do not rule out the possibility of the involvement of SL in final maturation, the results indicate that SL seems to be involved at least in energy and/or calcium metabolism during the spawning migration.     

Computer simulations of homeward-migrating Fraser River sockeye salmon: is compass orientation a sufficient direction-finding mechanism in the north-east Pacific Ocean?

Computer simulations were used to investigate whether compass orientation is a sufficient guidance mechanism for sockeye salmon migrating to the Fraser River from their ocean foraging grounds in the north-east Pacific Ocean. Daily surface ocean currents, simulated by the ocean surface current simulations (OSCURS) model, were used to test the influence of currents on the return oceanic migration of Fraser River sockeye salmon. High seas tagging and coastal recover data of Fraser River sockeye salmon were used for the migration simulations. Surface currents were shown to increase the speed of the homeward-migrating sockeye salmon, as well as to deflect the fish in a north-eastward direction. In spite of ocean currents, all Fraser River sockeye salmon were able to reach their destination with a fixed direction and bioenergetically efficient swimming speed when migration was delayed until the last month at sea. Compass orientation alone was shown to be a sufficient direction-finding mechanism for Fraser River sockeye salmon.